A three-dimensional topology of complex i inferred from evolutionary correlations

BMC Structural Biology

Volumn 12, Issue , 2012, Pages

  Kensche, Philip R ^a,b   Duarte, Isabel ^a,b   Huynen, Martijn A ^a,b  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b NETHERLANDS BIOINFORMATICS CENTRE   (Netherlands)

Author keywords

Assembly; Co evolution; Eukaryotic complex I; Mirror tree method; Quaternary topology

Indexed keywords

IRON; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SULFUR;

ACCURACY; ARTICLE; BINDING SITE; CONTROLLED STUDY; CORRELATION ANALYSIS; ENZYME LOCALIZATION; ENZYME SUBUNIT; EUKARYOTE; HUMAN; MEMBRANE; MOLECULAR EVOLUTION; MOLECULAR INTERACTION; MOLECULAR MODEL; NONHUMAN; PREDICTION; PROTEIN ASSEMBLY; PROTEIN QUATERNARY STRUCTURE; THERMUS THERMOPHILUS;

CONSERVED SEQUENCE; ELECTRON TRANSPORT COMPLEX I; EVOLUTION, MOLECULAR; HUMANS; MODELS, MOLECULAR; PROTEIN SUBUNITS; THERMUS THERMOPHILUS;

BACTERIA (MICROORGANISMS); EUKARYOTA; THERMUS THERMOPHILUS;

EID: 84864518996     PISSN: None     EISSN: 14726807     Source Type: Journal    
DOI: 10.1186/1472-6807-12-19     Document Type: Article

References (100)

1. Analysis of the subunit composition of complex I from bovine heart mitochondria. Carroll J, Fearnley IM, Shannon RJ, Hirst J, Walker JE, Mol Cell Proteomics 2003 2 2 117 126 10.1074/mcp.M300014-MCP200 12644575
2. The nuclear encoded subunits of complex I from bovine heart mitochondria. Hirst J, Carroll J, Fearnley IM, Shannon RJ, Walker JE, Biochim Biophys Acta 2003 1604 3 135 150 10.1016/S0005-2728(03)00059-8 12837546 (Pubitemid 36776747)
3. Contribution of each complex of the mitochondrial respiratory chain in the generation of the proton-motive force. Garcia-Vallve S, Biochem Mol Biol Edu 2004 32 1 17 19 10.1002/bmb.2004.494032010308 (Pubitemid 38124748)
4. Redox components and structure of the respiratory NADH:ubiquinone oxidoreductase (complex I). Friedrich T, Abelmann A, Brors B, Guénebaut V, Kintscher L, Leonard K, Rasmussen T, Scheide D, Schlitt A, Schulte U, et al. Biochim Biophys Acta 1998 1365 1-2 215 219 9693737 (Pubitemid 29359260)
5. The architecture of respiratory complex I. Efremov RG, Baradaran R, Sazanov LA, Nature 2010 465 7297 441 445 10.1038/nature09066 20505720
6. Functional modules and structural basis of conformational coupling in mitochondrial complex I. Hunte C, Zickermann V, Brandt U, Science 2010 329 5990 448 451 10.1126/science.1191046 20595580
7. Structure of the membrane domain of respiratory complex I. Efremov RG, Sazanov LA, Nature 2011 476 7361 414 420 10.1038/nature10330 21822288
8. Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus. Sazanov LA, Hinchliffe P, Science 2006 311 5766 1430 1436 10.1126/science.1123809 16469879 (Pubitemid 43376691)
9. Evolution of respiratory complex I: 'supernumerary' subunits are present in the -proteobacterial enzyme. Yip C-, Harbour ME, Jayawardena K, Fearnley IM, Sazanov LA, J Biol Chem 2010 286 7 5023 5033 21115482
10. Tracing the evolution of a large protein complex in the eukaryotes, NADH:ubiquinone oxidoreductase (Complex I). Gabaldán T, Rainey D, Huynen MA, J Mol Biol 2005 348 4 857 870 10.1016/j.jmb.2005.02.067 15843018 (Pubitemid 40544387)
11. The iron-sulphur protein Ind1 is required for effective complex I assembly. Bych K, Kerscher S, Netz DJA, Pierik AJ, Zwicker K, Huynen MA, Lill R, Brandt U, Balk J, EMBO J 2008 27 12 1736 1746 10.1038/emboj.2008.98 18497740
12. MidA is a putative methyltransferase that is required for mitochondrial complex I function. Carilla-Latorre S, Gallardo ME, Annesley SJ, Calvo-Garrido J, Grana O, Accari SL, Smith PK, Valencia A, Garesse R, Fisher PR, et al. J Cell Sci 2010 123 10 1674 1683 10.1242/jcs.066076 20406883
13. Involvement of two novel chaperones in the assembly of mitochondrial NADH:Ubiquinone oxidoreductase (complex I). Küffner R, Rohr A, Schmiede A, Krüll C, Schulte U, J Mol Biol 1998 283 2 409 417 10.1006/jmbi.1998.2114 9769214 (Pubitemid 28470418)
14. A molecular chaperone for mitochondrial complex I assembly is mutated in a progressive encephalopathy. Ogilvie I, Kennaway NG, Shoubridge EA, J Clin Invest 2005 115 10 2784 2792 10.1172/JCI26020 16200211 (Pubitemid 41434405)
15. A mitochondrial protein compendium elucidates complex I disease biology. Pagliarini DJ, Calvo SE, Chang B, Sheth SA, Vafai SB, Ong S-E, Walford GA, Sugiana C, Boneh A, Chen WK, et al. Cell 2008 134 1 112 123 10.1016/j.cell.2008. 06.016 18614015 (Pubitemid 351916708)
16. C6ORF66 is an assembly factor of mitochondrial complex I. Saada A, Edvardson S, Rapoport M, Shaag A, Amry K, Miller C, Lorberboum-Galski H, Elpeleg O, Am J Hum Genet 2008 82 1 32 38 10.1016/j.ajhg.2007.08.003 18179882 (Pubitemid 351735948)
17. Mutations in NDUFAF3 (C3ORF60), Encoding an NDUFAF4 (C6ORF66)-Interacting Complex I Assembly Protein, Cause Fatal Neonatal Mitochondrial Disease. Saada A, Vogel RO, Hoefs SJ, van den Brand MA, Wessels HJ, Willems PH, Venselaar H, Shaag A, Barghuti F, Reish O, et al. Am J Hum Genet 2009 84 718 727 10.1016/j.ajhg.2009.04.020 19463981
18. Mutation of C20orf7 disrupts complex I assembly and causes lethal neonatal mitochondrial disease. Sugiana C, Pagliarini DJ, McKenzie M, Kirby DM, Salemi R, Abu-Amero KK, Dahl H-HM, Hutchison WM, Vascotto KA, Smith SM, et al. Am J Hum Genet 2008 83 4 468 478 10.1016/j.ajhg.2008.09.009 18940309
19. Cytosolic signaling protein Ecsit also localizes to mitochondria where it interacts with chaperone NDUFAF1 and functions in complex I assembly. Vogel RO, Janssen RJRJ, van den Brand MAM, Dieteren CEJ, Verkaart S, Koopman WJH, Willems PHGM, Pluk W, van den Heuvel LPWJ, Smeitink JAM, et al. Genes Dev 2007 21 5 615 624 10.1101/gad.408407 17344420 (Pubitemid 46409475)
20. Human mitochondrial complex I assembles through the combination of evolutionary conserved modules: a framework to interpret complex I deficiencies. Ugalde C, Vogel R, Huijbens R, Heuvel BVD, Smeitink J, Nijtmans L, Hum Mol Genet 2004 13 20 2461 2472 10.1093/hmg/ddh262 15317750 (Pubitemid 39377850)
21. Co-evolution predicts direct interactions between mtDNA and nuclear DNA-encoded subunits of oxidative phosphorylation complex I. Gershoni M, Fuchs A, Shani N, Fridman Y, Corral-Debrinski M, Aharoni A, Frishman D, Mishmar D, J Mol Biol 2010 404 1 158 171 10.1016/j.jmb.2010.09.029 20868692
22. Mitochondrial NADH:ubiquinone oxidoreductase (complex I): proximity of the subunits of the flavoprotein and the iron-sulfur protein subcomplexes. Yamaguchi M, Hatefi Y, Biochemistry 1993 32 8 1935 1939 10.1021/bi00059a008 8448151 (Pubitemid 23086042)
23. Measuring genome evolution. Huynen MA, Bork P, Proc Natl Acad Sci U S A 1998 95 11 5849 5856 10.1073/pnas.95.11.5849 9600883 (Pubitemid 28248930)
24. Assigning protein functions by comparative genome analysis: protein phylogenetic profiles. Pellegrini M, Marcotte EM, Thompson MJ, Eisenberg D, Yeates TO, Proc Natl Acad Sci U S A 1999 96 8 4285 4288 10.1073/pnas.96.8.4285 10200254 (Pubitemid 29190328)
25. Lineage-specific gene loss following mitochondrial endosymbiosis and its potential for function prediction in eukaryotes. Gabaldán T, Huynen MA, Bioinformatics 2005 21 Suppl 2 i144 ii150 10.1093/bioinformatics/bti1124 16204094 (Pubitemid 41541732)
26. Practical and theoretical advances in predicting the function of a protein by its phylogenetic distribution. Kensche PR, van Noort V, Dutilh BE, Huynen MA, J R Soc Interface 2008 5 19 151 170 10.1098/rsif.2007.1047 17535793 (Pubitemid 350274448)
27. Similarity of phylogenetic trees as indicator of protein-protein interaction. Pazos F, Valencia A, Protein Eng 2001 14 9 609 614 10.1093/protein/14.9.609 11707606 (Pubitemid 33086280)
28. Correlated mutations and residue contacts in proteins. Göbel U, Sander C, Schneider R, Valencia A, Proteins 1994 18 4 309 317 10.1002/prot.340180402 8208723 (Pubitemid 24111530)
29. How frequent are correlated changes in families of protein sequences? Neher E, Proc Natl Acad Sci U S A 1994 91 1 98 102 10.1073/pnas.91.1.98 8278414 (Pubitemid 24018650)
30. Accurate prediction of protein-protein interactions from sequence alignments using a Bayesian method. Burger L, van Nimwegen E, Mol Syst Biol 2008 4 165 18277381
31. Identification of direct residue contacts in protein-protein interaction by message passing. Weigt M, White RA, Szurmant H, Hoch JA, Hwa T, Proc Natl Acad Sci U S A 2009 106 1 67 72 10.1073/pnas.0805923106 19116270
32. Mitochondrial proteome evolution and genetic disease. Huynen MA, de Hollander M, Szklarczyk R, Biochim Biophys Acta 2009 1792 12 1122 1129 10.1016/j.bbadis.2009.03.005 19328849
33. Coevolution study of mitochondria respiratory chain proteins: Toward the understanding of protein-protein interaction. Yang M, Ge Y, Wu J, Xiao J, Yu J, J Genet Genomics 2011 38 5 201 207 10.1016/j.jgg.2011.04.003 21621741
34. Assessing protein co-evolution in the context of the tree of life assists in the prediction of the interactome. Pazos F, Ranea JA, Juan D, Sternberg MJ, J Mol Biol 2005 352 4 1002 1015 10.1016/j.jmb.2005.07.005 16139301 (Pubitemid 41267084)
35. The inference of protein-protein interactions by co-evolutionary analysis is improved by excluding the information about the phylogenetic relationships. Sato T, Yamanishi Y, Kanehisa M, Toh H, Bioinformatics 2005 21 17 3482 3489 10.1093/bioinformatics/bti564 15994190 (Pubitemid 41235991)
36. High-confidence prediction of global interactomes based on genome-wide coevolutionary networks. Juan D, Pazos F, Valencia A, Proc Natl Acad Sci 2008 105 3 934 939 10.1073/pnas.0709671105 18199838 (Pubitemid 351282059)
37. BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. Criscuolo A, Gribaldo S, BMC Evol Biol 2010 10 1 210 10.1186/1471-2148-10-210 20626897
38. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Stamatakis A, Bioinformatics 2006 22 21 2688 2690 10.1093/bioinformatics/btl446 16928733 (Pubitemid 44642609)
39. Specificity in protein interactions and its relationship with sequence diversity and coevolution. Hakes L, Lovell SC, Oliver SG, Robertson DL, Proc Natl Acad Sci U S A 2007 104 19 7999 8004 10.1073/pnas.0609962104 17468399 (Pubitemid 47185865)
40. Evolutionary rate covariation reveals shared functionality and coexpression of genes. Clark NL, Alani E, Aquadro CF, Genome Res 2012 22 4 714 720 10.1101/gr.132647.111 22287101
41. Everitt BS, Dunn G, Applied multivariate data analysis / Brian S. Everitt and Graham Dunn Edward Arnold, London; Melbourne 1991
42. Supramolecular Organization of the Respiratory Chain in Neurospora crassa Mitochondria. Marques I, Dencher NA, Videira A, Krause F, Eukaryot Cell 2007 6 12 2391 2405 10.1128/EC.00149-07 17873079
43. Role of the Conserved Cysteine Residues of the 11.5 kDa Subunit in Complex I Catalytic Properties. Marques I, Ushakova AV, Duarte M, Videira A, J Biochem 2007 141 4 489 493 10.1093/jb/mvm049 17261544 (Pubitemid 351455296)
44. NADH:ubiquinone oxidoreductase from bovine heart mitochondria. cDNA sequences of the import precursors of the nuclear-encoded 39 kDa and 42 kDa subunits. Fearnley IM, Finel M, Skehel JM, Walker JE, Biochem J 1991 278 821 829 1832859
45. Tight binding of NADPH to the 39-kDa subunit of complex I is not required for catalytic activity but stabilizes the multiprotein complex. Biochimica et Biophysica Acta (BBA). Abdrakhmanova A, Zwicker K, Kerscher S, Zickermann V, Brandt U, Bioenergetics 2006 1757 12 1676 1682 10.1016/j.bbabio.2006.09.003 (Pubitemid 44841959)
46. Identification and characterization of a common set of complex I assembly intermediates in mitochondria from patients with complex I deficiency. Antonicka H, Ogilvie I, Taivassalo T, Anitori RP, Haller RG, Vissing J, Kennaway NG, Shoubridge EA, J Biol Chem 2003 278 44 43081 43088 10.1074/jbc.M304998200 12941961 (Pubitemid 37345924)
47. Characterization of the 9.5-kDa ubiquinone-binding protein of NADH:ubiquinone oxidoreductase (complex I) from Neurospora crassa. Heinrich H, Azevedo JE, Werner S, Biochemistry 1992 31 46 11420 11424 10.1021/bi00161a021 1445879
48. A scaffold of accessory subunits links the peripheral arm and the distal proton pumping module of mitochondrial complex I. Angerer H, Zwicker K, Wumaier Z, Sokolova L, Heide H, Steger M, Kaiser S, Nübel E, Brutschy B, Radermacher M, et al. Biochem J 2011 437 279 288 10.1042/BJ20110359 21545356
49. Disruption of the nuclear gene encoding the 20.8-kDa subunit of NADH: ubiquinone reductase of Neurospora mitochondria. da Silva MV, Alves PC, Duarte M, Mota N, da Cunha AL, Harkness TA, Nargang FE, Videira A, Mol Gen Genet 1996 252 1-2 177 183 8804391
50. Characterization of assembly intermediates of NADH:ubiquinone oxidoreductase (complex I) accumulated in Neurospora mitochondria by gene disruption. Nehls U, Friedrich T, Schmiede A, Ohnishi T, Weiss H, J Mol Biol 1992 227 4 1032 1042 10.1016/0022-2836(92)90519-P 1433284
51. Mutation Pressure and the Evolution of Organelle Genomic Architecture. Lynch M, Koskella B, Schaack S, Science 2006 311 5768 1727 1730 10.1126/science.1118884 16556832
52. Resolution of the membrane domain of bovine complex I into subcomplexes: implications for the structural organization of the enzyme. Sazanov LA, Peak-Chew SY, Fearnley IM, Walker JE, Biochemistry 2000 39 24 7229 7235 10.1021/bi000335t 10852722 (Pubitemid 30413113)
53. Subunit analysis of bovine heart complex I by reversed-phase high-performance liquid chromatography, electrospray ionization-tandem mass spectrometry, and matrix-assisted laser desorption/ionization-time-of-flight mass spectrometry. Lemma-Gray P, Valusová E, Carroll CA, Weintraub ST, Musatov A, Robinson NC, Anal Biochem 2008 382 2 116 121 10.1016/j.ab.2008.07.029 18721790
54. The 9.8 kDa Subunit of Complex I, Related to Bacterial Na+translocating NADH Dehydrogenases, is Required for Enzyme Assembly and Function in Neurospora crassa. Marques I, Duarte M, Videira A, J Mol Biol 2003 329 2 283 290 10.1016/S0022-2836(03)00443-1 12758076 (Pubitemid 36561584)
55. Structure and function of mitochondrial supercomplexes. Dudkina NV, Kouil R, Peters K, Braun H-P, Boekema EJ, Biochim Biophys Acta 2010 1797 6-7 664 670 20036212
56. Asymmetrical directional mutation pressure in the mitochondrial genome of mammals. Reyes A, Gissi C, Pesole G, Saccone C, Mol Biol Evol 1998 15 8 957 966 10.1093/oxfordjournals.molbev.a026011 9718723 (Pubitemid 28364449)
57. Codon usage is imposed by the gene location in the transcription unit. Delorme MO, Hénaut A, Curr Genet 1991 20 5 353 358 10.1007/BF00317061 1807825
58. Strand-specific nucleotide composition bias in echinoderm and vertebrate mitochondrial genomes. Asakawa S, Kumazawa Y, Araki T, Himeno H, Miura K, Watanabe K, J Mol Evol 1991 32 6 511 520 10.1007/BF02102653 1908022
59. New views on strand asymmetry in insect mitochondrial genomes. Wei S-J, Shi M, Chen X-X, Sharkey MJ, van Achterberg C, Ye G-Y, He J-H, PLoS One 2010 5 9 12708 10.1371/journal.pone.0012708 20856815
60. Mitochondrial genome diversity: evolution of the molecular architecture and replication strategy. Nosek J, Tomaska L, Curr Genet 2003 44 2 73 84 10.1007/s00294-003-0426-z 12898180 (Pubitemid 37441602)
61. Deviations from Chargaff's second parity rule in organellar DNA: Insights into the evolution of organellar genomes. Nikolaou C, Almirantis Y, Gene 2006 381 34 41 16893615 (Pubitemid 44468002)
62. Assembly of mitochondrial complex I and defects in disease. Lazarou M, Thorburn DR, Ryan MT, McKenzie M, Biochim Biophys Acta, Mol Cell Res 2009 1793 1 78 88 10.1016/j.bbamcr.2008.04.015 18501715
63. Human CIA30 is involved in the early assembly of mitochondrial complex I and mutations in its gene cause disease. Dunning CJR, McKenzie M, Sugiana C, Lazarou M, Silke J, Connelly A, Fletcher JM, Kirby DM, Thorburn DR, Ryan MT, EMBO J 2007 26 13 3227 3237 10.1038/sj.emboj.7601748 17557076 (Pubitemid 47057488)
64. Analysis of the assembly profiles for mitochondrial- and nuclear-DNA-encoded subunits into complex I. Lazarou M, McKenzie M, Ohtake A, Thorburn DR, Ryan MT, Mol Cell Biol 2007 27 12 4228 4237 10.1128/MCB.00074-07 17438127 (Pubitemid 46906548)
65. Investigation of the complex I assembly chaperones B17.2L and NDUFAF1 in a cohort of CI deficient patients. Vogel RO, van den Brand MAM, Rodenburg RJ, van den Heuvel LPWJ, Tsuneoka M, Smeitink JAM, Nijtmans LGJ, Mol Genet Metab 2007 91 2 176 182 10.1016/j.ymgme.2007.02.007 17383918 (Pubitemid 46765172)
66. Mutations in the Gene Encoding C8orf38 Block Complex I Assembly by Inhibiting Production of the Mitochondria-Encoded Subunit ND1. McKenzie M, Tucker EJ, Compton AG, Lazarou M, George C, Thorburn DR, Ryan MT, J Mol Biol 2011 414 3 413 426 10.1016/j.jmb.2011.10.012 22019594
67. Human Ind1, an Iron-Sulfur Cluster Assembly Factor for Respiratory Complex I. Sheftel AD, Stehling O, Pierik AJ, Netz DJA, Kerscher S, Elsasser H-P, Wittig I, Balk J, Brandt U, Lill R, Mol Cell Biol 2009 29 22 6059 6073 10.1128/MCB.00817-09 19752196
68. Subunits of Mitochondrial Complex I Exist as Part of Matrix- and Membrane-associated Subcomplexes in Living Cells. Dieteren CEJ, Willems PHGM, Vogel RO, Swarts HG, Fransen J, Roepman R, Crienen G, Smeitink JAM, Nijtmans LGJ, Koopman WJH, J Biol Chem 2008 283 50 34753 34761 10.1074/jbc.M807323200 18826940
69. The oxidized subunit B8 from human complex I adopts a thioredoxin fold. Brockmann C, Diehl A, Rehbein K, Strauss H, Schmieder P, Korn B, Kühne R, Oschkinat H, Structure 2004 12 9 1645 1654 10.1016/j.str.2004.06.021 15341729 (Pubitemid 39200517)
70. Energy converting NADH:quinone oxidoreductase (complex I). Brandt U, Annu Rev Biochem 2006 75 69 92 10.1146/annurev.biochem.75.103004.142539 16756485 (Pubitemid 44118026)
71. Structure, function, and formation of biological iron-sulfur clusters. Johnson DC, Dean DR, Smith AD, Johnson MK, Annu Rev Biochem 2005 74 247 281 10.1146/annurev.biochem.74.082803.133518 15952888 (Pubitemid 40995508)
72. Complex fate of paralogs. Szklarczyk R, Huynen M, Snel B, BMC Evol Biol 2008 8 1 337 10.1186/1471-2148-8-337 19094234
73. An integrated view of protein evolution. Pál C, Papp B, Lercher MJ, Nat Rev Genet 2006 7 5 337 348 10.1038/nrg1838 16619049
74. A single determinant dominates the rate of yeast protein evolution. Drummond DA, Raval A, Wilke CO, Mol Biol Evol 2006 23 2 327 337 16237209 (Pubitemid 43100047)
75. High-resolution protein complexes from integrating genomic information with molecular simulation. Schug A, Weigt M, Onuchic JN, Hwa T, Szurmant H, Proc Natl Acad Sci U S A 2009 106 52 22124 22129 10.1073/pnas.0912100106 20018738
76. Direct-coupling analysis of residue coevolution captures native contacts across many protein families. Morcos F, Pagnani A, Lunt B, Bertolino A, Marks DS, Sander C, Zecchina R, Onuchic JN, Hwa T, Weigt M, Proc Natl Acad Sci U S A 2011 108 49 1293 E1301 10.1073/pnas.1111471108 22106262
77. Correlated mutations via regularized multinomial regression. Sreekumar J, ter Braak CJ, van Ham RC, van Dijk AD, BMC Bioinforma 2011 12 444 10.1186/1471-2105-12-444
78. Disentangling direct from indirect co-evolution of residues in protein alignments. Burger L, van Nimwegen E, PLoS Comput Biol 2010 6 1 1000633 10.1371/journal.pcbi.1000633 20052271
79. In silico two-hybrid system for the selection of physically interacting protein pairs. Pazos F, Valencia A, Proteins 2002 47 2 219 227 10.1002/prot.10074 11933068 (Pubitemid 34263334)
80. Database resources of the National Center for Biotechnology Information. Wheeler DL, Barrett T, Benson DA, Bryant SH, Canese K, Chetvernin V, Church DM, DiCuccio M, Edgar R, Federhen S, et al. Nucleic Acids Res 2006 35 suppl 1 5 D12 17170002
81. Protein homology detection by HMM-HMM comparison. Söding J, Bioinformatics 2005 21 7 951 960 10.1093/bioinformatics/bti125 15531603 (Pubitemid 40467915)
82. EMBOSS: The European Molecular Biology Open Software Suite. Rice P, Longden I, Bleasby A, Trends Genet 2000 16 6 276 277 10.1016/S0168-9525(00) 02024-2 10827456
83. Recent developments in the MAFFT multiple sequence alignment program. Katoh K, Toh H, Brief Bioinform 2008 9 4 286 298 10.1093/bib/bbn013 18372315 (Pubitemid 351890825)
84. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Thompson JD, Higgins DG, Gibson TJ, Nucleic Acids Res 1994 22 22 4673 4680 10.1093/nar/22.22.4673 7984417 (Pubitemid 24354800)
85. ClustalW-MPI: ClustalW analysis using distributed and parallel computing. Li K-B, Bioinformatics 2003 19 12 1585 1586 10.1093/bioinformatics/btg192 12912844 (Pubitemid 37038879)
86. Profile hidden Markov models. Eddy SR, Bioinformatics 1998 14 9 755 763 10.1093/bioinformatics/14.9.755 9918945 (Pubitemid 28552108)
87. Strang G, Introduction to Linear Algebra Wellesley-Cambridge Press, In. 1998
88. Correlated evolution of interacting proteins: looking behind the mirrortree. Kann MG, Shoemaker BA, Panchenko AR, Przytycka TM, J Mol Biol 2009 385 1 91 98 10.1016/j.jmb.2008.09.078 18930732
89. R Development Core Team, R: A Language and Environment for Statistical Computing R Foundation for Statistical Computing, Vienna, Austria 2011
90. Borg I, Groenen PJF, Modern Multidimensional Scaling Theory and Applications, Springer 2005
91. Prediction of protein residue contacts with a PDB-derived likelihood matrix. Singer MS, Vriend G, Bywater RP, Protein Eng 2002 15 9 721 725 10.1093/protein/15.9.721 12456870 (Pubitemid 35470428)
92. FactoMineR: An R Package for Multivariate Analysis. Lê S, Josse J, Husson F, J Stat Softw 2008 25 1 1 18
93. Human mitochondrial complex I assembly: a dynamic and versatile process. Vogel RO, Smeitink JAM, Nijtmans LGJ, Biochim Biophys Acta 2007 1767 10 1215 1227 10.1016/j.bbabio.2007.07.008 17854760 (Pubitemid 47498312)
94. Definition of the nuclear encoded protein composition of bovine heart mitochondrial complex I. Identification of two new subunits. Carroll J, Shannon RJ, Fearnley IM, Walker JE, Hirst J, J Biol Chem 2002 277 52 50311 50317 10.1074/jbc.M209166200 12381726 (Pubitemid 36042179)
95. GRIM-19, a cell death regulatory gene product, is a subunit of bovine mitochondrial NADH:ubiquinone oxidoreductase (complex I). Fearnley IM, Carroll J, Shannon RJ, Runswick MJ, Walker JE, Hirst J, J Biol Chem 2001 276 42 38345 38348 10.1074/jbc.C100444200 11522775
96. Towards a proteome-scale map of the human protein-protein interaction network. Rual J-F, Venkatesan K, Hao T, Hirozane-Kishikawa T, Dricot A, Li N, Berriz GF, Gibbons FD, Dreze M, Ayivi-Guedehoussou N, et al. Nature 2005 437 7062 1173 1178 10.1038/nature04209 16189514 (Pubitemid 41509356)
97. Oxidative Damage to Mitochondrial Complex I Due to Peroxynitrite. Murray J, Taylor SW, Zhang B, Ghosh SS, Capaldi RA, J Biol Chem 2003 278 39 37223 37230 10.1074/jbc.M305694200 12857734 (Pubitemid 37175238)
98. Adaptive selection of mitochondrial complex I subunits during primate radiation. Mishmar D, Ruiz-Pesini E, Mondragon-Palomino M, Procaccio V, Gaut B, Wallace DC, Gene 2006 378 11 18 16828987 (Pubitemid 44108461)
99. Acyl-CoA dehydrogenase 9 is required for the biogenesis of oxidative phosphorylation complex I. Nouws J, Nijtmans L, Houten SM, van den Brand M, Huynen M, Venselaar H, Hoefs S, Gloerich J, Kronick J, Hutchin T, et al. Cell Metab 2010 12 3 283 294 10.1016/j.cmet.2010.08.002 20816094
100. The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Szklarczyk D, Franceschini A, Kuhn M, Simonovic M, Roth A, Minguez P, Doerks T, Stark M, Muller J, Bork P, Nucleic Acids Res 2011 39 Database issue 561 568 21045058